Proteins in the gas phase

Wiley Interdisciplinary Reviews: Computational Molecular Science

Volumn 3, Issue 4, 2013, Pages 408-425

  Meyer, Tim ^a   Gabelica, Valérie ^b   Grubmüller, Helmut ^a   Orozco, Modesto ^c,d  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AQUEOUS ENVIRONMENT; EXPERIMENTAL APPROACHES; GAS-PHASE MEASUREMENT; SOURCES OF INFORMATIONS; STRUCTURAL CHANGE; STRUCTURAL INFORMATION; STRUCTURAL STUDIES; THEORETICAL RESEARCH;

GASES;

PROTEINS;

EID: 84879105528     PISSN: 17590876     EISSN: 17590884     Source Type: Journal    
DOI: 10.1002/wcms.1130     Document Type: Article

References (125)

1. Dill KA. Dominant forces in protein folding. Biochemistry 1990, 29:7133-7155.
2. Barron LD, Hecht L, Wilson G. The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure. Biochemistry 1997, 36:13143-13147.
3. Neutze R, Huldt G, Hajdu J, van der Spoel D. Potential impact of an X-ray free electron laser on structural biology. Radiation Phys Chem 2004, 71:905-916.
4. Chapman HN, Barty A, Bogan MJ, Boutet S, Frank M, Hau-Riege SP, Marchesini S, Woods BW, Bajt S, Benner WH, et al. Femtosecond diffractive imaging with a soft-X-ray free-electron laser. Nat Phys 2006, 2:839-843.
5. Barrera NP, Robinson CV. Advances in the mass spectrometry of membrane proteins: from individual proteins to intact complexes. Annu Rev Biochem 2011, 80:247-271.
6. Gabelica V, De Pauw E, Rosu F. Interaction between antitumor drugs and a double-stranded oligonucleotide studied by electrospray ionization mass spectrometry. J Mass Spectrom 1999, 34:1328-1337.
7. Rosu F, Gabelica V, Houssier C, Colson P, Pauw ED. Triplex and quadruplex DNA structures studied by electrospray mass spectrometry. Rapid Commun Mass Spectrom 2002, 16:1729-1736.
8. Benesch JLP, Robinson CV. Biological chemistry: dehydrated but unharmed. Nature 2009, 462:576-577.
9. Yin S, Loo JA. Top-down mass spectrometry of supercharged native protein-ligand complexes. Int J Mass Spectrom 2011, 300:118-122.
10. Park AY, Robinson CV. Protein-nucleic acid complexes and the role of mass spectrometry in their structure determination. Crit Rev Biochem Mol Biol 2011, 46:152-164.
11. Fuerstenau SD, Benner WH, Thomas JJ, Brugidou C, Bothner B, Siuzdak G. Mass spectrometry of an intact virus. Angew Chem Int Ed 2001, 40:541-544.
12. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. Electrospray ionization for mass spectrometry. Science 1989, 246:64-71.
13. Fenn JB, Mann M, Meng CK, Wong SF. Electrospray ionization-principles and practice. Mass Spectrom Rev 1990, 9:37-70.
14. Nemes P, Marginean I, Vertes A. Spraying mode effect on droplet formation and ion chemistry in electrosprays. Anal Chem 2007, 79:3105-3116.
15. Luedtke WD, Landman U, Chiu YH, Levandier DJ, Dressler RA, Sok S, Gordon MS. Nanojets, electrospray, and ion field evaporation: molecular dynamics simulations and laboratory experiments. J Phys Chem A 2008, 112:9628-9649.
16. Kebarle P. A brief overview of the present status of the mechanisms involved in electrospray mass spectrometry. J Mass Spectrom 2000, 35:804-817.
17. Kebarle P, Peschke M. On the mechanisms by which the charged droplets prodced by electrospray lead to gas phase ions. Anal Chim Acta 2000, 406:11-35.
18. Znamenskiy V, Marginean I, Vertes A. Solvated ion evaporation from charged water nanodroplets. J Phys Chem A 2003, 107:7406-7412.
19. Hogan CJ, Carroll JA, Rohrs HW, Biswas P, Gross ML. Combined charged residue-field emission model of macromolecular electrospray ionization. Anal Chem 2009, 81:369-377.
20. Fenn JB. Ion formation from charged droplets: roles of geometry, energy and time. J Am Soc Mass Spectrom 1993, 4:524-535.
21. Felitsyn N, Peschke M, Kebarle P. Origin and number of charges observed on multiply-protonated native proteins produced by ESI. Int J Mass Spectrom 2002, 219:39-62s.
22. Hautreux M, Hue N, Du Fou de Kerdaniel A, Zahir A, Malec V, Laprévote O. Under non-denaturing solvent conditions, the mean charge state of a multiply charged protein ion formed by electrospray is linearly correlated with the macromolecular surface. Int J Mass Spectrom 2004, 231:131-137.
23. Iavarone AT, Jurchen JC, Williams ER. Supercharged protein and peptide ions formed by electrospray ionization. Anal Chem 2001, 73:1455-1460.
24. Fernandez De la Mora J. Electrospray ionization of large multiply charged species proceeds via Dole's charged residue mechanism. Anal Chim Acta 2000, 406:93-104.
25. Testa L, Brocca S, Grandori R. Charge-surface correlation in electrospray ionization of folded and unfolded proteins. Anal Chem 2011, 83:6459-6463.
26. Sterling HJ, Cassou CA, Trnka MJ, Burlingame AL, Krantz BA, Williams ER. The role of conformational flexibility on protein supercharging in native electrospray ionization. Phys Chem Chem Phys 2011, 13:18288-18296.
27. Sterling HJ, Kintzer AF, Feld GK, Cassou CA, Krantz BA, Williams ER. Supercharging protein complexes from aqueous solution disrupts their native conformations. J Am Soc Mass Spectrom 2012, 23:191-200.
28. Ahadi E, Konermann L. Modeling the behavior of coarse-grained polymer chains in charged water droplets: implications for the mechanism of electrospray ionization. J Phys Chem B 2012, 116:104-112.
29. Collette C, De Pauw E. Calibration of the internal energy distribution of ions produced by electrospray. Crit Rev Biochem Mol Biol 1998, 12:165-170.
30. Bagal D, Kitova EN, Liu L, El-Hawiet A, Schnier PD, Klassen JS. Gas phase stabilization of noncovalent protein complexes formed by electrospray ionization. Anal Chem 2009, 81:7801-7806.
31. Schnier PD, Gross DS, Williams ER. On the maximum charge state and proton transfer reactivity of peptide and protein ions formed by electrospray ionization. J Am Soc Mass Spectrom 1995, 6:1086-1097.
32. Marchese R, Grandori R, Carloni P, Raugei S. On the zwitterionic nature of gas-phase peptides and protein ions. PLoS Comput Biol 2010, 6.
33. Schnier PD, Gross DS, Williams ER. Electrostatic forces and dielectric polarizability of multiply protonated gas-phase cytochrome c ions probed by ion/molecule chemistry. J Am Chem Soc 1995, 117:6747-6757.
34. Miteva M, Demirev PA, Karshikoff AD. Multiply-protonated protein ions in the gas phase: calculation of the electrostatic interactions between charged sites. J Phys Chem B 1997, 101:9645-9650.
35. Meyer T, de la Cruz X, Orozco M. An atomistic view to the gas phase proteome. Structure 2009, 17:88-95.
36. Valentine SJ, Clemmer DE. Temperature-dependent H/D exchange of compact and elongated cytochrome c ions in the gas phase. J Am Soc Mass Spectrom 2002, 13:506-517.
37. Mao Y, Woenckhaus J, Kolafa J, Ratner MA, Jarrold MF. Thermal unfolding of unsolvated cytochrome c: experiment and molecular dynamics simulations. J Am Chem Soc 1999, 121:2712-2721.
38. Prasad M, Conforti PF, Garrison BJ, Yingling YG. Computational investigation into the mechanisms of UV ablation of poly(methyl methacrylate). Appl Surf Sci 2007, 253:6382-6385.
39. Jaskolla T, Karas M. Compelling evidence for lucky survivor and gas phase protonation: the unified MALDI analyte protonation mechanism. J Am Soc Mass Spectrom 2011, 22:976-988.
40. Heck AJR, van den Heuvel RHH. Investigation of intact protein complexes by mass spectrometry. Mass Spectrom Rev 2004, 23:368-389.
41. Berkenkamp S, Karas M, Hillenkamp F. Ice as a matrix for IR-matrix-assisted laser desorption/ionization: mass spectra from a protein single crystal. PNAS 1996, 93:7003-7007.
42. Morgner N, Kleinschroth T, Barth H-D, Ludwig B, Brutschy B. A novel approach to analyze membrane proteins by laser mass spectrometry: from protein subunits to the integral complex. J Am Soc Mass Spectrom 2007, 18:1429-1438.
43. Charvat A, Abel B. How to make big molecules fly out of liquid water: applications, features and physics of laser assisted liquid phase dispersion mass spectrometry. Phys Chem Chem Phys 2007, 9:3335.
44. Wattenberg A, Sobott F, Brutschy B. Detection of intact hemoglobin from aqueous solution with laser desorption mass spectrometry. Crit Rev Biochem Mol Biol 2000, 14:859-861.
45. Wiederschein F. Investigation of Laser-Induced-Liquid-Beam-Ion-Desorption (LILBID) with Molecular Dynamics Simulations. PhD Dissertation. Göttingen, Germany: University of Göttingen; 2009.
46. Breuker K, McLafferty FW. The thermal unfolding of native cytochrome c in the transition from solution to gas phase probed by native electron capture dissociation. Angew Chem Int Ed 2005, 44:4911-4914.
47. Cooper HJ, Hakansson K, Marshall AG. The role of electron capture dissociation in biomolecular analysis. Mass Spectrom Rev 2005, 24:201-222.
48. Breuker K, Brüschweiler S, Tollinger M. Electrostatic stabilization of a native protein structure in the gas phase. Angew Chem Int Ed 2011, 50:873-877.
49. Hemling ME, Conboy JJ, Bean MF, Mentzer M, Carr SA. Gas phase H/D exchange in electrospray ionization mass spectrometry as a practical tool for structure elucidation. J Am Soc Mass Spectrom 1994, 5:434-442.
50. Wood TD, Chorush RA, Wampler FM III, Little DP, O'Connor PB, McLafferty FW. Gas-phase folding and unfolding of cytochrome c cations. Proc Natl Acad Sci USA 1995, 92:2451-2454.
51. Wyttenbach T, Bowers MT. Gas phase conformations of biological molecules: the hydrogen/deuterium exchange mechanism. J Am Soc Mass Spectrom 1999, 10:9-14.
52. Robinson EW, Williams ER. Multidimensional separations of ubiquitin conformers in the gas phase: relating ion cross sections to H/D exchange measurements. J Am Soc Mass Spectrom 2005, 16:1427-1437.
53. Wang F, Freitas MA, Marshall AG, Sykes BD. Gas-phase memory of solution-phase protein conformation: H/D exchange and Fourier transform ion cyclotron resonance mass spectrometry of the N-terminal domain of cardiac troponin C. Int J Mass Spectrom 1999, 192:319-325.
54. Eyler JR. Infrared multiple photon dissociation spectroscopy of ions in Penning traps. Mass Spectrom Rev 2009, 28:448-467.
55. Polfer N, Oomens J. Vibrational spectroscopy of bare and solvated ionic complexes of biological relevance. Mass Spectrom Rev 2009, 28:468-494.
56. Antoine R, Dugourd P. Visible and ultraviolet spectroscopy of gas phase protein ions. Phys Chem Chem Phys 2011, 13:16494-16509.
57. Iavarone AT, Patriksson A, van der Spoel D, Parks JH. Fluorescence probe of Trp-cage protein conformation in solution and in gas phase. J Am Chem Soc 2007, 129:6726-6735.
58. Banerjee S, Mazumdar S. Electrospray ionization mass spectrometry: a technique to access the information beyond the molecular weight of the analyte. Int J Anal Chem 2012, 2012:1-40.
59. Vonderach M, Ehrler OT, Matheis K, Karpuschkin T, Papalazarou E, Brunet C, Antoine R, Weis P, Hampe O, Kappes MM, Dugourd P. Probing electrostatic interactions and structural changes in highly charged protein polyanions by conformer-selective photoelectron spectroscopy. Phys Chem Chem Phys 2011, 13:15554-15558.
60. Garand E, Kamrath MZ, Jordan PA, Wolk AB, Leavitt CM, McCoy AB, Miller SJ, Johnson MA. Determination of noncovalent docking by infrared spectroscopy of cold gas-phase complexes. Science 2012, 335:694-698.
61. Nagornova NS, Rizzo TR, Boyarkin OV. Interplay of intra- and intermolecular H-bonding in a progressively solvated macrocyclic peptide. Science 2012, 336:320-323.
62. Papadopoulos G, Svendsen A, Boyarkin OV, Rizzo TR. Conformational distribution of bradykinin [bk + 2 H](2+) revealed by cold ion spectroscopy coupled with FAIMS. J Am Soc Mass Spectrom 2012.
63. Revercomb HE, Mason EA. Theory of plasma chromatography/gaseous electrophoresis-a review. Anal Chem 1975, 47:970-983.
64. Chapman HN, Fromme P, Barty A, White TA, Kirian RA, Aquila A, Hunter MS, Schulz J, DePonte DP, Weierstall U, et al. Femtosecond X-ray protein nanocrystallography. Nature 2011, 470:73-77.
65. Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 2010, 466:329-333.
66. Black DM, Payne AH, Glish GL. Determination of cooling rates in a quadrupole ion trap. J Am Soc Mass Spectrom 2006, 17:932-938.
67. Dunbar RC. BIRD (blackbody infrared radiative dissociation): evolution, principles, and applications. Mass Spectrom Rev 2004, 23:127-158.
68. McLuckey SA. Principles of collisional activation in analytical mass spectrometry. J Am Soc Mass Spectrom 1991, 3:599-614.
69. Wang B, Valentine S, Plasencia M, Raghuraman S, Zhang X. Artificial neural networks for the prediction of peptide drift time in ion mobility mass spectrometry. BMC Bioinformatics 2010, 11:182.
70. Morsa D, Gabelica V, De Pauw E. Effective temperature of ions in traveling wave ion mobility spectrometry. Anal Chem 2011, 83:5775-5782.
71. Merenbloom SI, Flick TG, Williams ER. How hot are your ions in TWAVE ion mobility spectrometry? J Am Soc Mass Spectrom 2012, 23:553-562.
72. Drahos L, Heeren RMA, Collette C, De Pauw E, Vékey K. Thermal energy distribution observed in electrospray ionization. J Mass Spectrom 1999, 34:1373-1379.
73. Takats Z, Drahos L, Schlosser G, Vékey K. Feasibility of formation of hot ions in electrospray. Anal Chem 2002, 74:6427-6429.
74. Hall Z, Politis A, Bush MF, Smith LJ, Robinson CV. Charge-state dependent compaction and dissociation of protein complexes: insights from ion mobility and molecular dynamics. J Am Chem Soc 2012, 134:3429-3438.
75. Arcella A, Portella G, Ruiz ML, Eritja R, Vilaseca M, Gabelica V, Orozco M. Structure of triplex DNA in the gas phase. J Am Chem Soc 2012, 134:6596-6606.
76. Mesleh MF, Hunter JM, Shvartsburg AA, Schatz GC, Jarrold MF. Structural information from ion mobility measurements: effects of the long-range potential. J Phys Chem 1996, 100:16082-16086.
77. Wyttenbach T, von Helden G, Batka JJ Jr, Carlat D, Bowers MT. Effect of the long-range potential on ion mobility measurements. J Am Soc Mass Spectrom 1997, 8:275-282.
78. Bohrer BC, Mererbloom SI, Koeniger SL, Hilderbrand AE, Clemmer DE. Biomolecule analysis by ion mobility spectrometry. In: Annual Review of Analytical Chemistry. Vol 1. Palo Alto, CA: Annual Reviews; 2008, 293-327.
79. Jurneczko E, Barran PE. How useful is ion mobility mass spectrometry for structural biology? The relationship between protein crystal structures and their collision cross-sections in the gas phase. Analyst 2011, 136:20-28.
80. Sun J, Kitova EN, Klassen JS. Method for stabilizing protein-ligand complexes in nanoelectrospray ionization mass spectrometry. Anal Chem 2006, 79:416-425.
81. Barrera NP, Di Bartolo N, Booth PJ, Robinson CV. Micelles protect membrane complexes from solution to vacuum. Science 2008, 321:243-246.
82. Sun J, Kitova EN, Klassen JS. Method for stabilizing protein-ligand complexes in nanoelectrospray ionization mass spectrometry. Anal Chem 2006, 79:416-425.
83. Sharon M, Ilag LL, Robinson CV. Evidence for micellar structure in the gas phase. J Am Chem Soc 2007, 129:8740-8746.
84. Friemann R, Larsson DSD, Wang Y, van der Spoel D. Molecular dynamics simulations of a membrane protein-micelle complex in vacuo. J Am Chem Soc 2009, 131:16606-16607.
85. Wang Y, Larsson DSD, van der Spoel D. Encapsulation of myoglobin in a cetyl trimethylammonium bromide micelle in vacuo: a simulation study. Biochemistry 2009, 48:1006-1015.
86. Caleman C, van der Spoel D. Temperature and structural changes of water clusters in vacuum due to evaporation. J Chem Phys 2006, 125:154508-154508-9.
87. Marklund EG, Larsson DSD, van der Spoel D, Patriksson A, Caleman C. Structural stability of electrosprayed proteins: temperature and hydration effects. Phys Chem Chem Phys 2009, 11:8069-8078.
88. Jarrold MF. Helices and sheets in vacuo. Phys Chem Chem Phys 2007, 9:1659.
89. Mark P, Nilsson L. Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. J Phys Chem A 2001, 105:9954-9960.
90. Gao J, Luque FJ, Orozco M. Induced dipole moment and atomic charges based on average electrostatic potentials in aqueous solution. J Chem Phys 1993, 98:2975-2982.
91. Rueda M, Kalko SG, Luque FJ, Orozco M. The structure and dynamics of DNA in the gas phase. J Am Chem Soc 2003, 125:8007-8014.
92. Orozco M, Tirado-Rives J, Jorgensen WL. Mechanism for the rotamase activity of FK506 binding protein from molecular dynamics simulations. Biochemistry 1993, 32:12864-12874.
93. Blom MN, Compagnon I, Polfer NC, von Helden G, Meijer G, Suhai S, Paizs B, Oomens J. Stepwise solvation of an amino acid: the appearance of zwitterionic structures. J Phys Chem A 2007, 111:7309-7316.
94. Kjeldsen F, Silivra OA, Zubarev RA. Zwitterionic states in gas-phase polypeptide ions revealed by 157-nm ultra-violet photodissociation. Chemistry 2006, 12:7920-7928.
95. Mao Y, Ratner MA, Jarrold MF. Molecular dynamics simulations of the charge-induced unfolding and refolding of unsolvated cytochrome c. J Phys Chem B 1999, 103:10017-10021.
96. Patriksson A, Marklund E, van der Spoel D. Protein structures under electrospray conditions. Biochemistry 2007, 46:933-945.
97. Peng Y, Voth GA. Expanding the view of proton pumping in cytochrome c oxidase through computer simulation. Biochim Biophys Acta 2012, 1817:518-525.
98. Lill MA, Helms V. Molecular dynamics simulation of proton transport with quantum mechanically derived proton hopping rates (Q-HOP MD). J Chem Phys 2001, 115:7993-8005.
99. Ahadi E, Konermann L. Ejection of solvated ions from electrosprayed methanol/water nanodroplets studied by molecular dynamics simulations. J Am Chem Soc 2011, 133:9354-9363.
100. Kong X, Brooks CL. λ-Dynamics: a new approach to free energy calculations. J Chem Phys 1996, 105:2414.
101. Donnini S, Tegeler F, Groenhof G, Grubmüller H. Constant pH molecular dynamics in explicit solvent with λ-dynamics. J Chem Theory Comput 2011, 7:1962-1978.
102. Wolynes PG. Biomolecular folding in vacuo!!!(?). Proc Natl Acad Sci USA 1995, 92:2426-2427.
103. Skinner O, McLafferty F, Breuker K. How ubiquitin unfolds after transfer into the gas phase. J Am Soc Mass Spectrom 2012, 23:1011-1014.
104. Patriksson A, Adams CM, Kjeldsen F, Zubarev RA, van der Spoel D. A direct comparison of protein structure in the gas and solution phase: the Trp-cage. J Phys Chem B 2007, 111:13147-13150.
105. Dugourd P, Antoine R, Breaux G, Broyer M, Jarrold MF. Entropic stabilization of isolated β-sheets. J Am Chem Soc 2005, 127:4675-4679.
106. Wyttenbach T, Bowers MT. Structural stability from solution to the gas phase: native solution structure of ubiquitin survives analysis in a solvent-free ion mobility-mass spectrometry environment. J Phys Chem B 2011, 115:12266-12275.
107. Shelimov KB, Jarrold MF. Conformations, unfolding, and refolding of apomyoglobin in vacuum: an activation barrier for gas-phase protein folding. J Am Chem Soc 1997, 119:2987-2994.
108. Li J, Taraszka JA, Counterman AE, Clemmer DE. Influence of solvent composition and capillary temperature on the conformations of electrosprayed ions: unfolding of compact ubiquitin conformers from pseudonative and denatured solutions. Int J Mass Spectrom 1999, 185-187:37-47.
109. Koeniger SL, Merenbloom SI, Sevugarajan S, Clemmer DE. Transfer of structural elements from compact to extended states in unsolvated ubiquitin. J Am Chem Soc 2006, 128:11713-11719.
110. Pierson NA, Chen L, Valentine SJ, Russell DH, Clemmer DE. Number of solution states of bradykinin from ion mobility and mass spectrometry measurements. J Am Chem Soc 2011, 133:13810-13813.
111. Arteca GA, Tapia O. Structural transitions in neutral and charged proteins in vacuo. J Mol Graph Model 2001, 19:102-118.
112. van der Spoel D, Marklund EG, Larsson DSD, Caleman C. Proteins, lipids, and water in the gas phase. Macromol Biosci 2011, 11:50-59.
113. Ben-Tal N, Sitkoff D, Topol IA, Yang A-S, Burt SK, Honig B. Free energy of amide hydrogen bond formation in vacuum, in water, and in liquid alkane solution. J Phys Chem B 1997, 101:450-457.
114. Sugita Y, Okamoto Y. Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 1999, 314:141-151.
115. Baumketner A. Amyloid beta-protein monomer structure: a computational and experimental study. Protein Sci 2006, 15:420-428.
116. Wolynes PG, Onuchic JN, Thirumalai D. Navigating the folding routes. Science 1995, 267:1619-1620.
117. Levinthal C. How to fold graciously. In: Mossbauer Spectroscopy in Biological Systems. Proceedings of a meeting held at Allerton House. Urbana: University of Illinois Press; 1969, 22-24.
118. Onuchic JN, Luthey-Schulten Z, Wolynes PG. Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 1997, 48:545-600.
119. Ortiz AR, Strauss CEM, Olmea O. MAMMOTH (matching molecular models obtained from theory): an automated method for model comparison. Protein Sci 2002, 11:2606-2621.
120. D'Abramo M, Meyer T, Bernadó P, Pons C, Recio JF, Orozco M. On the use of low-resolution data to improve structure prediction of proteins and protein complexes. J Chem Theory Comput 2009, 5:3129-3137.
121. Koeniger SL, Clemmer DE. Resolution and structural transitions of elongated states of ubiquitin. J Am Soc Mass Spectrom 2007, 18:322-331.
122. Bowman GR, Huang X, Pande VS. Using generalized ensemble simulations and Markov state models to identify conformational states. Methods 2009, 49:197-201.
123. Noé F, Schütte C, Vanden-Eijnden E, Reich L, Weikl TR. Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations. PNAS 2009, 106:19011-19016.
124. Bowman GR, Pande VS. Protein folded states are kinetic hubs. PNAS 2010, 107:10890-10895.
125. Voelz VA, Bowman GR, Beauchamp K, Pande VS. Molecular simulation of ab initio protein folding for a millisecond folder NTL9(1-39). J Am Chem Soc 2010, 132:1526-1528.